The Rest of the Story: Take-all Decline with Continuous Wheat Monoculture

Of all the advances in root disease management over the past 40 years, none is more counter intuitive than the discovery and exploitation of the spontaneous decline in the root disease, take-all (caused by the soilborne fungus, Gaeumannomyces graminis var. tritici) with continuous wheat and barley sequences. For this commentary, I have chosen to tell the novel story behind the story of take-all decline.

Transfer of suppressive soil from one field to another.

Dr. Peter Shipton from the U.K had joined me at WSU Pullman for 2 years starting in early 1969, and together we set out to see whether a factor or factors responsible for take-all decline could be transferred from one field to another. The late Elvin Kulp as Extension Agronomist for Grant County, WA directed us to a field near Quincy, WA that was in the 12th year of monoculture winter wheat—with no take-all in spite of irrigation known to favor this disease. Shipton, Richard Smiley (then my PhD student) and I loaded garbage cans with soil from that field and soil from an adjacent site still under sage brush and hauled it in the fall of 1969 to the WSU station at Puyallup, WA. There, we sprinkled these and several other soils onto replicate plots, roto-tilled the plots to a depth of 6 inches. The actual amount of introduced soil mixed into the plots amounted to only about 0.5% by weight. We then planted the experimental area uniformly winter wheat, with the take-all fungus as colonized oat grains mixed with a high-quality wheat seed in the drill box so that the inoculum went directly into the seed furrow with the seed.

The 1st crop was devastated by take-all, with no benefit of added soil. We then reseeded the plot area with winter wheat but with no more inoculum of the take-all pathogen, so that the only inoculum in the soil was the infected roots and crowns from the 1st crop. Remarkably, take all was virtually nonexistent in all four (and only these four) replicate plots of the 2nd crop where soil from the Quincy wheat field had been added 18 months earlier (plants on the right), but was still severe in plots with no soil amendment (far left) or amended with soil from the non-cropped site next to the 12-year-monoculture wheat field (plants in the center). Even more remarkable, wheat was uniformly healthy border to border in the 3rd year of winter wheat, in spite of the large amount of carry over pathogen inoculum from the 1st and especially the 2nd wheat crop. Clearly, something in soil from the field in continuous wheat monoculture was suppressive to take-all, was transferable and it could multiply. Also with this experiment, we knew that take-all decline was not some figment of our imagination.

Documentation of the role of antibiotic-producing bacteria in take-all decline.

Thanks to world-class research by David Weller, Linda Thomashow and their graduate students, post-doctoral associates and technical assistants, take-all decline is now understood to result from one or a select few genotypes of root-associated bacteria of Pseudomonas fluorescens that 1) inhibit the take-all pathogen by production of the antibiotic 2,4-diacetylphloroglucinol (DAPG) and 2) buildup in response to one or more outbreaks of take-all and continuous monoculture of wheat and barley. In a symbiotic way, these novel bacteria, responding to an ecological niche of infected roots, team up with and protect roots so as to give the equivalent of disease-resistant plants.

Many distinct genotypes of DAPG-producing P. fluorescens bacteria have since been identified world-wide, with just one of them consistently associated with take-all decline in Washingto State. More recent studies suggest that other DAPG-producing genotypes, or strains with ability to produce other antibiotics, tend to respond spontaneously to other crops and cropping systems. Considering the diversity of these root-associated bacteria as revealed by the DAPG-producing genotypes, one can only imagine the permutations and combinations of crop and root-associated bacteria and their roles in sustaining yields that otherwise could only be achieved with a more traditional long and diverse crop rotation.

The emergence of the research unit focused on biological control of root pathogens.

Never imagining where this research would lead, looking back, it provided 1) justification for hiring David Weller in 1979, Linda Thomashow in 1985, and establishment of the ARS Root Disease and Biological Control Research Unit at Pullman in 1984; 2) a model system for a modernized science of biological control of soilborne plant pathogens; 3) clues to the success of intensive cropping systems as illustrated with monoculture cereals; and 4) the centerpiece of an integrated approach to management of all four root diseases in cereal-intensive direct-seed cropping systems oin the U.S Pacific Northwest that includes timely green bridge management, fertilizer placement with some soil disturbance and trash clearance in the seed row, and use of fresh wheat seed treated with a chemical for protection against Pythium.

Research on take-all decline has been funded during some 3 decades by the USDA competitive grants program—starting with my first grant in 1978 that allowed me to hire David Weller as my postdoctoral associate. Aspects of this research were carried out in cooperation with growers in six counties (Grant, Skagit, Spokane, Walla Walla and Whitman in WA and Umatilla, OR) and on six WSU research farms (Lind, Mt. Vernon, Palouse Conservation Field Station, Plant Pathology, Puyallup, Spillman). An experiment on Spillman Agronomy Farm with bacteria-treated winter wheat in 1987/88 involved an antibiotic-producing strain engineered to express a color marker and represented the first field release of a genetically engineered organism in the Pacific Northwest.

Take-all decline in the 15th year of continuous wheat monoculture.

The longest running experiment is on the Lind station where winter and spring wheat sequences have grown continuously under irrigation in a 1-ha plot since 1967; take-all was severe by the 7th year of continuous monoculture wheat, as revealed by the striking responses to disease control by soil fumigation (below), but thereafter, declined gradually until, by the 15th year the crop in the same 1-field was the same whether the soil had been fumigated prior to planting (to the man’s left) or left natural (to the man’s right).

Intensive if not continuous monoculture cereals widely practiced in the Palouse.

A drive through the Palouse region of eastern Washington and adjacent northern Idaho where annual precipitation is sufficient for annual cropping, one sees almost exclusively cereals, with only the occasional field of peas, lentils, and more likely chick peas (garbanzo beans) in the rotation. Some fields have been in continuous cereals for 20 or more years, including with no-till (direct seed). Typically winter wheat is rotated with either spring wheat or spring barley, which helps to manage weeds and the crop residue. Weller has a test for the antibiotic-producing bacteria that build up to provide biological control of take-all, and finds populations in the range of 6 log units and higher per a standard length or weight of root in long-term cereals monoculture fields, compared with 4 logs or lower in fields where take-all has been controlled by crop rotation and the soil still conducive to the disease.

Take-all decline managed with continuous cereals is now the center piece of an integrated system that includes fresh seed treated for protection against Pythium and Rhizoctonia, effective and timely management of volunteer cereals in the stubble after harvest, and band fertilizer close enough to the seed row so even plants with any one of the root rots can still access nutrients, especially the relatively immobile phosphorus. (See also Root Diseases of Wheat and Barley: What do they look like and what do they do to the crop?